A Rapid Method to Assess Grape Rust Mites on Leaves and
Observations from Case Studies in Western Oregon Vineyards
Schreiner, R. P., Skinkis, P. A., & Dreves, A. J. (2014). A Rapid Method to Assess
Grape Rust Mites on Leaves and Observations from Case Studies in Western
Oregon Vineyards. HortTechnology, 24(1), 38-47.
American Society for Horticultural Science
Version of Record
http://hdl.handle.net/1957/47976
http://cdss.library.oregonstate.edu/sa-termsofuse
A Rapid Method to Assess Grape Rust Mites on
Leaves and Observations from Case Studies in
Western Oregon Vineyards
R. Paul Schreiner1,4, Patricia A. Skinkis2, and Amy J. Dreves3
ADDITIONAL INDEX WORDS. Calepitrimerus vitis, Eriophyidae, extraction method,
leaf stippling, scouting technique, Vitis vinifera
SUMMARY. The grape rust mite [Calepitrimerus vitis (Acari: Eriophyidae)] is an
important pest of grapevines (Vitis sp.) in grape-growing regions around the world.
A rapid method for extracting eriophyoid mites was adapted from earlier studies to
provide integrated pest management (IPM) consultants and commercial growers
with a practical, efficient, and reliable tool to monitor grape rust mites in vineyards
and nursery stock vines. The rinse in bag (RIB) method allows quick extraction of
mites from young shoots or from leaves using 35% to 70% ethanol or isopropanol in
a sealable plastic bag. The RIB method recovered 85% of grape rust mites from
single leaves in the first rinse. The method is useful to estimate grape rust mites on
young shoots (£10 cm length), although recovery of grape rust mites (average
ranging from 35% to 81%) was lower because of a higher density of trichomes on
young shoots as compared with leaf samples. The RIB method was not effective to
assess grape rust mites within dormant buds, so a separate method using a blender to
disrupt tissues and extract mites in alcohol was developed. The RIB method was
used to determine grape rust mite abundance with leaf symptoms in commercial
vineyards and nursery stock vines. The earliest visible symptom of grape rust mite
damage on leaves in the summer was the development of stippling that is distinct
from the type of damage caused by other grapevine pests. The stippling is described
as numerous clear zones of small diameter (resembling pinholes) that are visible
when a leaf is backlit. The severity of stippling was related to the number of grape
rust mites present on leaves, with >600 occurring on leaves with severe stippling
symptoms. In commercial vineyard case studies, the RIB method was used over two
seasons and revealed that grape rust mite populations remained on leaves until
postharvest, and foliar applications of wettable sulfur reduced grape rust mite
populations on leaves.
T
he grape rust mite can attain
high populations on grapevine
shoots and leaves in Europe,
Australia, and North and South America
(Duso et al., 2010), where it feeds by
inserting a stylet into epidermal layers of
plant cells (Westphal and Manson,
1996). Grape rust mites overwinter
We thank Matthew Scott, Morgan Curtis, Karen
Peterson, and Alison Reeve for technical assistance,
and Allen Holstein, Jaime Cantu, Robert Schultz,
Luke Pedotti, and Ken Johnston for providing access
to vineyards, cooperating with sampling, and providing spray records at vineyards sampled.
Mention of trade names or commercial products in
this publication is solely for the purpose of providing
specific information and does not imply recommendation or endorsement by the U.S. Department of
Agriculture.
1
U.S. Department of Agriculture—Agriculture Research Service Horticultural Crops Research Laboratory, 3420 Northwest Orchard Avenue, Corvallis, OR
97330
2
Department of Horticulture, Oregon State University, 4017 ALS Building, Corvallis, OR 97331
3
Department of Crop and Soil Science, Oregon State
University, 109 Crop Science Building, Corvallis, OR
97331
4
Corresponding author. E-mail: Paul.Schreiner@ars.
usda.gov.
38
in and around individual dormant
buds, and in the bark of older woody
tissues (Bernard et al., 2005; PérezMoreno and Moraza-Zorrilla, 1998).
The impact of grape rust mites on
vine growth can be severe when very
high populations (>500 grape rust
mites per shoot) are present early in
the growing season and when cool
temperatures in spring reduce the rate
of shoot expansion (Bernard et al.,
2005). Stunting of spring shoot growth
is cultivar dependent, with fast growing
cultivars being less affected by grape
rust mite outbreaks. The pest status of
the grape rust mite is unclear in some
regions where infestation has not
caused apparent damage to leaves or
shoots (Duso et al., 2010) possibly
because of different environmental conditions and the populations of predatory mites that feed on grape rust mites.
Earlier research conducted in western
Oregon suggested that very low numbers (<10 grape rust mites per shoot)
may cause retarded spring shoot
growth (Walton et al., 2007). However, subsequent sampling in numerous
vineyards where spring shoot stunting
occurred (2005 to 2009) revealed the
absence of grape rust mites or grape
bud mites (Colomerus vitis) on young
shoots (R.P. Schreiner and P.A. Skinkis,
unpublished data), suggesting that
other factors can be responsible for
restricted growth including winter
freeze damage (Fennel, 2004), cool
early season temperatures (Winkler
et al., 1974), boron deficiency (Cook,
1966), herbicide damage (Bhatti et al.,
1997), and high numbers of western
flower thrips [Frankliniella occidentalis (McNally et al., 1985)].
More recently (2009 to 2012),
a large number of newly planted vineyards in the Willamette Valley developed stunted, deformed, and often
pubescent shoots during spring, and
these stunted shoots had high numbers of grape rust mites (>500 mites
per shoot), similar to levels that caused
stunting in Australian vineyards
(Bernard et al., 2005). The high incidence of stunted shoots and presence
of grape rust mites in newly planted
vineyards in the region led producers
to prophylactic use of early season
miticides, including application of lime
sulfur during wooly bud stage and
budbreak, even though the presence
of grape rust mites was not confirmed
at most sites. Because of prior studies
Units
To convert U.S. to SI,
multiply by
U.S. unit
SI unit
To convert SI to U.S.,
multiply by
29.5735
0.3048
9.3540
2.54
25.4
6.4516
1.1209
1
1
(F – 32) O 1.8
fl oz
ft
gal/acre
inch(es)
inch(es)
inch2
lb/acre
micron
ppm
F
mL
m
Lha–1
cm
mm
cm2
kgha–1
mm
mLL–1
C
0.0338
3.2808
0.1069
0.3937
0.0394
0.1550
0.8922
1
1
(C · 1.8) + 32
•
February 2014 24(1)
associating grape rust mite presence
with spring stunting, many producers
and consultants assumed that any
spring growth abnormalities were
caused by grape rust mites without
verifying their presence. The lack of
confirmation of pest presence was due
in part to the difficulty in monitoring
grape rust mites. As with many eriophyoid mites, monitoring grape rust
mite populations in plant tissues is
difficult because of their microscopic
size (80 to 360 mm) and often-cryptic
lifestyle (Monfreda et al., 2010).
At the same time that severe
mite outbreaks occurred in vineyards, new grapevine plants received
from nurseries or propagated from
dormant canes collected from local
vineyards developed stippling symptoms on leaves (10% of vines)
shortly after plants were moved into
the greenhouse, and these stippled
leaves had moderate populations of
grape rust mites (50 to 150 per leaf).
A small percentage of vines (3%)
also developed stunted and unusually
pubescent shoots where high numbers of grape rust mites were localized (>200 per shoot). Grape rust
mites were extracted from these
shoots and leaves using an ethanol
washing technique [henceforth referred to as the spray and sieve
(S&S) method] and retrieved on
a 25-mm sieve as described by others
(Pérez-Moreno and Moraza-Zorrilla,
1998; Zacharda et al., 1988). Fauna
were then examined under a stereoscope. This method was shared with
local producers who used it to monitor
grape rust mites in a number of recently
planted vineyards. However, after consultation with those producers, it became clear that a more efficient method
was necessary. The overall goal of this
research was to develop a practical,
economical, and efficient technique to
allow viticulturists and agricultural
IPM consultants to assess grape rust
mite populations. The rinse in bag
method was developed to meet this
need. Procedural aspects of the RIB
method were examined and compared
with both direct visual counts of mites
on plant tissues and to ethanol extracts
after disrupting tissues in a blender.
The RIB method was also used to
examine seasonal populations of grape
rust mites in commercial vineyards and
to establish the relationship of visual
symptoms on leaves to grape rust mite
abundance.
•
February 2014 24(1)
Materials and methods
EXPERIMENTAL SITES. Three vineyards were used for testing in 2011
and 2012. Vineyard 1, located near
Salem, OR, was planted in 2009 to
‘Pinot noir’ (Vitis vinifera) grafted to
3309C rootstock (Vitis riparia · Vitis
rupestris). Vines were spaced 4 ft
apart in row and 6 ft between rows in
north-south oriented rows, were spur
pruned to a cordon system with a terminal arced cane at the last node
position, and the canopy was vertically
shoot positioned. This vineyard was
used to test different aspects of the
RIB extraction method in 2011 as the
site was found to be severely infested
with grape rust mites (>3000 per leaf).
The vineyard manager first observed
leaves showing stippling symptoms in
early July. The manager used the S&S
extraction method and a stereoscope
to quantify grape rust mite populations at this vineyard. In addition, leaf
samples were collected from Vineyard
1 to test the RIB method in midsummer (22 Aug.) and again in late
summer (19 Sept.) of 2011 to examine
the impact of canopy applications
of sulfur or an insecticidal soap (see
below) applied by the grower. Both
bronzing and stippling were observed
on leaves at this vineyard in 2011, but
no stunted shoots were found in
Spring 2011 or 2012.
Vineyard 2, located in Dayton,
OR, was planted in 2008 to ‘Chardonnay’ (V. vinifera) grafted to Riparia
Gloire rootstock (V. riparia). Vines
were spaced 5 ft apart in row and 7 ft
between rows in north-south oriented
rows, were cane pruned, and trained to
a vertically shoot-positioned trellis system. Within this particular vineyard
block, vines had moderate grape rust
mite infestation (100 to 400 per leaf)
throughout 2011. This site was used to
relate leaf stippling symptoms with grape
rust mite abundance (13 July 2011),
and to test the utility of scouting for
stippled leaves to identify grape rust mite
presence (12 Sept. 2011). Grape rust
mite populations on young shoots and
leaves were also monitored in this vineyard over two growing seasons (2011
and 2012). Pesticide spray records for
this site were provided by the vineyard
manager from 2009 to 2012. Dormant
canes with buds were also collected from
this site to develop a blender method to
examine grape rust mites overwintering
in or around individual buds.
Vineyard 3 is a block within the
same commercial vineyard as Vineyard 2, and they are located within
300 m of each other. This block was
planted in 2009 to ‘Syrah’ (V. vinifera) grafted to Riparia Gloire rootstock. Vines were spaced 5 ft apart in
row and 7 ft between rows in north–
south oriented rows, cane pruned,
and trained to a vertically shootpositioned trellis system. This vineyard was only used in 2012 to sample
grape rust mites on young shoots
after abnormally stunted shoots were
noticed by the vineyard manager after
budbreak. Young shoots were collected and compared from both Vineyard 2 and Vineyard 3 in 2012.
Mite extraction methods
SPRAY & SIEVE. The S&S method
based on previous ethanol washing procedures (Pérez-Moreno and MorazaZorrilla, 1998; Zacharda et al., 1988)
was initially used for quantifying grape
rust mites on leaves and tissues. The
method was modified by vigorously
spraying the leaf surface with ethanol
or isopropanol (at 70% v/v) using a
manual atomizer pump sprayer. The
front and back of each leaf was held at
a 45 angle over a 25-mm sieve while
spraying with alcohol solution to retrieve grape rust mites and other fauna.
Contents of the sieve were transferred
to a petri dish using an alcohol solution and examined under a stereoscope
at ·40 magnification. Gridded petri
dishes were used when high numbers
of mites (>200) were found in a given
sample, and a random subset of grids
was counted and a multiplication factor used to calculate the total grape
rust mites present. The three most
commonly found fauna groups included grape rust mites, predatory
mites (Typhlodromus pyri), and western flower thrips, and each group was
counted in all samples extracted.
RINSE IN BAG. A second method,
RIB, was developed that used readily
available supplies. This method was
evaluated and compared with the
S&S method. Individual leaves were
collected in the field into individual
resealable plastic bags. The RIB
method was used to extract all fauna
from single leaves or single shoots
directly in the bag in which they were
collected. Leaf blades were cut into
2 cm2 pieces and returned to the
original collection bag. For small
shoots, leaves were cut from the main
39
RESEARCH REPORTS
stem and the main stem was cut into
1 cm lengths using small scissors
and returned to the collection bag. A
total of 50 mL of either 35% or 70%
ethanol or isopropanol was added to
the bag while rinsing the scissors. The
bag was resealed and shaken vigorously for 30 s. A small hole was cut
from the corner of the bag and the
rinsate was decanted into a petri dish
leaving the plant tissues behind.
Grape rust mites, predatory mites,
and western flower thrips were
counted under a stereoscope, as described earlier. The small volume of
alcohol used for this method eliminates the sieve step and resulted in less
alcohol use as compared with the S&S
method. The only specialized equipment required for this method is
a stereoscope with a magnification
range of at least ·40, although ·100
is preferable.
BLENDER METHOD—YOUNG
SHOOTS. Because leaf tissue is covered
with trichomes, and young shoots can
have very high trichome density early
in the season (Liakopoulos et al.,
2006), we anticipated that the RIB
method would not efficiently extract
grape rust mites from young shoots.
A standard laboratory blender was
used to disrupt tissues and collect
fauna released on a series of sieves.
After mites were extracted from
young shoots using the RIB method,
plant tissues and any fauna remaining
in the bag were transferred to
a blender cup with 50 to 100 mL of
70% ethanol, blended for 10 s on high
speed using a blender (Waring Laboratory Science, Winsted, CT), and
transferred to a series of sieves (500,
250, 125, and 25 mm). The material
on each sieve was thoroughly washed
with cold tap water, transferred with
70% ethanol to petri dishes, and fauna
therein were counted under a stereoscope. This method resulted in more
plant debris in the rinsate and required more time to sort through
debris under the stereoscope.
B LENDER METHOD — DORMANT
BUDS. The RIB method was not effective for assessing grape rust mites
in buds during dormancy because
they were most often located under
bud scales or deep within the leaf scar
area below dormant buds. The
blender method was used to assess
grape rust mites present in and
around dormant buds. Single buds
were removed from the cane by
40
cutting into the woody tissue 2 to
3 mm surrounding and below each
bud and included the necrotic tissue
around the leaf scar. The bud was
then bisected longitudinally, placed
in the blender with 50 mL of 70%
ethanol, blended on high speed for
10 s, and fauna were collected on
125- and 25-mm sieves.
VISUAL COUNTS. Direct visual
counts were performed by carefully
examining young shoots, leaves, or
buds under a stereoscope, gently pulling back trichomes, and separating
tiny new leaves with forceps. For
dormant buds, the bud scales were
sequentially removed to examine underlying tissues. This method was
useful in determining the location of
grape rust mites in different tissues,
but it was difficult to generate accurate counts and was exceptionally
time-consuming.
Sampling methods and tests
performed
COMPARISON
OF VINE SYMPTOMS
TO GRAPE RUST MITES USING THE RIB
AND S&S METHOD. About 150 individual leaves were randomly collected from the middle to upper
canopy from numerous locations
throughout Vineyard 1 on 22 Aug.
2011. Roughly 30% to 40% of the
leaves in this vineyard displayed either
bronzing or stippling symptoms.
Each leaf was placed in a single plastic
bag upon collection, placed in a cooler,
transported to the laboratory, and
stored at 4 C. After initial inspection
under a stereoscope to confirm presence of grape rust mites, leaves were
sorted and placed into three categories
based upon leaf symptoms: bronzed,
stippled, or asymptomatic. Twenty
bronzed leaves were randomly selected and ten were extracted using
either the RIB method or S&S
method with 70% isopropanol to compare methods. Another set of 24
bronzed leaves were then extracted
with the RIB method using either
35% or 70% isopropanol (n = 12), to
test if concentration of alcohol influenced grape rust mite extraction. A
third set of 20 leaves was extracted
with 35% isopropanol using the RIB
method to determine difference in
fauna between leaves showing either
stippling or bronzing symptoms
(n = 10). Grape rust mites, predatory
mites, and western flower thrips were
quantified in all extracts. Extraction
efficiency of the RIB method was determined from five individual bronzed
leaves with high grape rust mite numbers and extracting three consecutive
times with fresh 35% isopropanol
(50 mL) for each leaf. Leaves were
carefully examined under a stereoscope
after the third extraction in the bag
confirming that no grape rust mites
remained on the leaves.
ASSOCIATION OF SYMPTOMATIC
LEAVES TO GRAPE RUST MITES. Leaf
samples were collected on 13 July and
12 Sept. 2011 from Vineyard 2 to test
the relationship of leaf stippling
symptoms with the presence of grape
rust mites. On 13 July, 100 fully
expanded leaves were randomly collected from midcanopy throughout
the vineyard, placed in individual
resealable plastic bags, placed in a
cooler for transit, and stored at 4 C
until analysis. Individual leaves were
rated for the severity of stippling
damage using a category scale from
0 to 4 (0 = no symptoms, 1 = 10% to
20% leaf surface with pinhole stippling, 2 = 20% to 40% leaf surface
with pinhole stippling, 3 = more than
40% leaf surface with pinhole stippling and clear zones coalescing and
forming zones 1–2 mm in size, 4 =
more than 50% leaf surface with pinhole stippling and clear zones coalescing and forming zones >2 mm in
size). Leaves were backlit and photographed. Grape rust mites and other
fauna were extracted from leaves using the S&S method and counted
under a stereoscope. A minimum of
eight leaves in each symptom category were extracted from the July
samples. Leaves were again collected
in September by using two collection
methods. On 12 Sept., 30 fully
expanded leaves from the mid to
upper canopy were collected at random, and another 30 leaves were
collected based on the presence of
stippling symptoms observed in the
field. Leaves from both collection
methods were individually bagged
and transported to the laboratory as
described earlier. Fourteen leaves of
each type were randomly selected and
extracted using the RIB method with
35% isopropanol. Grape rust mites,
predatory mites, and western flower
thrips were counted in all extracts.
RIB METHOD EFFICACY ON YOUNG
SHOOTS. Young shoots were collected
from Vineyard 2 on 30 Apr. 2012,
•
February 2014 24(1)
15 d after budbreak. Both normal
shoots and those that were stunted
were selected throughout the block.
Stunted shoots in Vineyard 2 lacked
the pubescent symptoms found earlier in heavily grape rust mite-infested
vineyards, but were visibly shorter
than most in the vineyard. Shoots
from Vineyard 3 were collected on 2
May 2012, 10 d after budbreak.
Both normal shoots and those that
were stunted and highly pubescent
were selected. All shoots were individually bagged and handled as mentioned earlier. Individual shoots were
first measured for length and examined under a stereoscope to quantify
the number of grape rust mites, predatory mites, and western flower thrips
within a 5-min time limit. Immediately thereafter, fauna were extracted
using the RIB method with 50 mL of
70% ethanol. Following RIB extraction, each shoot was transferred to
a blender and remaining fauna were
extracted using the blender method
for shoots. The number of grape rust
mites, predatory mites, and western
flower thrips was subsequently
counted. The percent recovery of
grape rust mites using the RIB
method was calculated based on the
total count of grape rust mites from
the RIB method plus blender method
for each shoot.
COMPARISON OF BLENDER
M ETH OD T O V ISU A L CO U N TS ON
DORMANT BUDS. Dormant canes were
collected in Vineyard 2 from four
different locations within the vineyard
on 13 Jan. 2012. Two canes were
randomly selected from each vineyard
location, transported back to the laboratory, and a single cane from each
vineyard location was randomly
assigned to visual examination or
blender extraction for a total of four
canes used for each method. The
blender method could not be compared
with visual counts on the same buds
because buds were destroyed during the
process. The number of grape rust mites
was recorded for each bud along the
cane from the basal most bud (node 1)
to the 14th node. No time limit was
applied when counting grape rust mites
under the stereoscope for buds.
A CASE STUDY OF GRAPE RUST
MITE SEASONAL POPULATIONS. Population estimates of grape rust mites at
a moderately infested block at Vineyard 2 were carried out over 2 years
(2011 and 2012). Whole shoots were
•
February 2014 24(1)
collected shortly after budbreak (19
May 2011 and 30 Apr. 2012) when
shoots were 7 to 12 cm long, and
leaves were sampled during early
summer (13 July 2011 and 14 June
2012) and again before (13 Sept.
2011 and 6 Sept. 2012) and after
fruit harvest (6 Oct. 2011 and 8
Oct. 2012). At each sample date,
50 young shoots or 50 single leaves
were collected at random throughout
the canopy and vineyard block without scouting for symptoms. Sampling
was conducted in this way to avoid
any bias because of the presence of
stippling symptoms and to best estimate grape rust mite abundance in
the vineyard. Grape rust mites were
extracted using the RIB method with
35% isopropanol from 20 single
shoots or 20 leaves per sampling date.
Sulfur was applied multiple times to
the entire vineyard in each year for
dual use as a miticide and fungicide,
although spray applications varied
by year. In 2011, wettable sulfur
(ThiosperseÒ 80; Continental Sulfur
Co., Kilgore, TX) was applied to vines
on 17 Apr., 3 May, 27 June, 3 Aug.,
and 17 Aug. at a rate of 4 lb/acre
actual sulfur. In addition, the first two
sprays in 2011 (17 April and 3 May)
included lime sulfur (28% calcium
polysulfide; OR-CAL, Junction City,
OR) at 0.2 gal/acre rate. In 2012,
wettable sulfur was applied on 24 Apr.,
7 May, 29 May, 9 July, 17 July, 26 July,
and 6 Aug. at the same rate as 2011,
but no lime sulfur was used in 2012.
A CASE STUDY OBSERVING THE
IMPACT FROM SPRAYS ON GRAPE RUST
MITES. The impact of midseason miticides to control grape rust mites was
tested commercially by the vineyard
manager at Vineyard 1 in 2011. Vines
were sprayed with wettable sulfur
(Microthiol DisperssÒ 80WP; United
Phosphorus, King of Prussia, PA) at
5 lb/acre actual sulfur along with
an adjuvant (Vintre OilÒ; Oro Agro,
Fresno, CA), or with potassium salts
of fatty acids (M-PedeÒ; Dow AgroSciences, Indianapolis, IN) at a rate of
0.75 gal/acre a.i. on 22 Aug. 2011. A
20-row section of the vineyard was
left as a nontreated control, receiving
no sprays. The spray application was
not spatially replicated, but prior sampling within each of the areas of the
vineyard indicated high grape rust
mite abundance. Fifteen leaves were
randomly collected from the mid and
upper canopy within each of the three
treatment areas (sulfur, potassium
salts of fatty acids, and nontreated),
individually bagged, and transported
to the laboratory on 19 Sept. 2011,
1 month after spray application.
Grape rust mites, predatory mites,
and western flower thrips were quantified using the RIB method with 35%
isopropanol. Because significant leaf
damage was observed during the
grape-ripening phase, the impact of
grape rust mites on vine photosynthesis was examined. Single leaf gas
exchange was measured 3 d after sampling (22 Sept. 2011) by selecting
both midcanopy (older) and upper
canopy (younger) leaves that were
either bronzed or asymptomatic in
a 2 · 2 factorial design. Twelve sunexposed leaves were measured within
each category (total of 48 leaves)
using a portable photosynthesis system
(6400 XTR; LI-COR Biosciences,
Lincoln, NE) under clear, cloudless
conditions in early afternoon (1350
to 1440 HR) using ambient sunlight
(PAR > 1500 mmolm–2s–1) with temperature (30.6 C) and carbon dioxide
(CO2) control (400 ppm).
STATISTICAL ANALYSIS. The number of grape rust mites, predatory mites,
and western flower thrips extracted by
various methods or numbers from visual counts on shoots, buds, or leaves,
as well as the leaf area or shoot length
data were analyzed by analysis of variance (ANOVA) or by the nonparametric Kruskal–Wallis test for those data
that could not be transformed to satisfy
variance assumptions for ANOVA. The
statistical test used for a given dataset is
indicated in the tables or figure legends,
and effects were considered significant
at P £ 0.05. Means were compared
using Tukey’s honestly significant difference test when ANOVA was used or
by Kruskal–Wallis multiple comparison tests at 95% confidence. Means
are reported for each group of categorical data, except for the grape rust
mite numbers associated with varying levels of leaf stippling symptoms
at Vineyard 2 because these data were
log-transformed to overcome homogeneity of variance assumptions before
ANOVA. Back-transformed means and
95% confidence intervals are reported
for these data.
Results
COMPARISON
OF VINE SYMPTOMS
TO GRAPE RUST MITES USING THE RIB
AND
S&S METHOD. The RIB method
41
RESEARCH REPORTS
was equally effective as the modified
S&S method for extracting grape rust
mites and predatory mites from single
leaves at Vineyard 1 (Table 1). However, the RIB method extracted more
western flower thrips than the S&S
method from leaves. There was no
difference in the number of fauna
extracted from leaves when comparing 35% to 70% isopropanol with the
RIB method. Also, the numbers of
grape rust mites or predatory mites on
bronzed and stippled leaves were similar, although more western flower
thrips were found on stippled leaves.
Although we did not formally quantify the time needed to process samples with the RIB and S&S methods,
the RIB method took 50% less time
to process samples than the S&S
method. The RIB method was efficient in grape rust mite extraction
even when samples were highly infested by grape rust mites. Assuming
that all mites were extracted after
three washes from five individual
leaves, the average recovery of grape
rust mites in the first wash was 85%
(Fig. 1). Examination of leaves under
the stereoscope after the third successive wash confirmed that no grape
rust mites remained on these leaves,
although it is likely that a few grape
rust mites were not extracted or
visually detected. About 20% of the
leaves examined from Vineyard 1 had
more than 5000 grape rust mites
inhabiting a single leaf, causing significant visual symptoms of stippling
and bronzing.
ASSOCIATION OF SYMPTOMATIC
LEAVES TO GRAPE RUST MITES. The
number of grape rust mites increased
with the severity of leaf stippling
symptoms from ‘Chardonnay’ leaves
collected in early summer (Fig. 2).
Leaves with a severity rating of 1, 2, 3,
or 4 had mean grape rust mite numbers of 19, 112, 274, and 568, respectively. When Vineyard 2 leaves
were sampled late in summer using
stippling symptoms to guide leaf selection, about 5-fold more grape rust
mites per leaf were found compared
with leaves collected at random (Table 2). The numbers of western
flower thrips and predatory mites
were similar for collections of symptomatic and random leaf samples.
RIB METHOD EFFICACY ON YOUNG
SHOOTS. The number of grape rust
mites extracted from normal shoots
of ‘Chardonnay’ grapevines from
42
Table 1. Effect of extraction method, isopropanol concentration, and leaf
symptoms on the mean number of fauna extracted from individual ‘Pinot noir’
grapevine leaves from Vineyard 1 on 22 Aug. 2011.
Method/treatment
Rinse in bag methodz
Spray and sieve method
P level
35% Isopropanolx
70% Isopropanol
P level
Bronzed leavesx
Stippled leaves
P level
Grape rust mites
Predatory mites
3576
3659
0.931
3261
3914
0.461
3944
4112
0.877
7.6
8.6
0.862
9.4
8.1
0.762
5.3
7.5
0.573
Western flower
thrips
4.5 ay
0.9 b
0.008
7.9
11.1
0.452
5.0 b
12.8 a
0.006
z
Bronzed leaves were used to compare extraction methods (n = 10).
Means followed by a different letter for mites or western flower thrips within each test category differ based on
Tukey’s honestly significant difference test at 95% confidence.
x
The rinse in bag method was used to compare isopropanol concentrations (n = 12) and leaves with different
symptoms (n = 10).
y
Fig. 1. Recovery of grape rust mites from five individual ‘Pinot noir’ grapevine
leaves in three successive extractions of 50 mL (1.7 fl oz) using the rinse in bag
method with 35% isopropanol. Leaves were collected from Vineyard 1 on 22 Aug.
2011.
Vineyard 2 in early Spring 2012 did
not differ from the number found on
stunted shoots for any of the methods
tested (Table 3). Mean grape rust
mite numbers were numerically
higher on stunted shoots, but high
variability was observed using all
methods. The RIB and RIB + blender
counts of grape rust mites were
higher than direct counts. The number of predatory mites on normal
shoots was greater than that on
stunted shoots, although the number
of western flower thrips did not differ
among shoot types. The efficiency of
grape rust mite extraction using the
RIB method was generally high
(>68%) for shoots from Vineyard 2.
Stunted ‘Syrah’ shoots (Fig. 3) collected from Vineyard 3 in Spring
2012 had significantly more grape
rust mites than the normal shoots
for each of the methods used (Table
3). The number of grape rust mites
extracted using the RIB method or
the combined total (RIB + blender)
was 16-fold greater in stunted
shoots than in normal shoots.
Stunted ‘Syrah’ shoots also had more
western flower thrips as compared
with normal shoots, but predatory
mite numbers did not differ. The
efficiency of grape rust mite extraction using the RIB method was lower
for ‘Syrah’ shoots (35% to 40%) as
compared with ‘Chardonnay’ shoots,
most likely because of the greater
number of trichomes present. ‘Chardonnay’ shoots were more glabrous
and broke bud earlier in the season,
leading to earlier shoot expansion and
lower trichome density, presumably
•
February 2014 24(1)
Fig. 2. Association between grape rust mites extracted from individual
‘Chardonnay’ grapevine leaves and leaf stippling symptoms in early summer.
Leaf stippling severity was rated on a scale from 0 to 4, and grape rust mites were
extracted with 70% ethanol using the spray and sieve method. Data presented
are back-transformed means and 95% confidence limits from log-transformed data.
Leaves were collected from Vineyard 2 on 13 July 2011.
Table 2. Effect of leaf sampling method on the mean number of fauna extracted
from individual ‘Chardonnay’ grapevine leaves from Vineyard 2 on 12 Sept.
2011.
Leaf sampling methodz
Symptomatic
Random
Variable
Stippling severity rating (0–4 scale)
Grape rust mites
Predatory mites
Western flower thrips
Leaf area (cm2) w
1.7 a
3070 a
5.8
0.9
99
x
0.5 b
594 b
4.6
0.9
110
P levely
<0.001
0.005*
1.000*
0.988
0.425
z
Leaves were collected by selecting leaves with stippling symptoms or at random. Samples were extracted using the
rinse in bag method with 35% isopropanol.
y
Probability values followed by * were derived from Kruskal–Wallis (K-W) analysis, all others from analysis of
variance.
x
Means followed by a different letter in a row differ based on Tukey’s honestly significant difference test or K-W
multiple range test at 95% confidence (n = 14).
w
1 cm2 = 0.1550 inch2.
Fig. 3. Photographs of normal and stunted shoots of ‘Syrah’ grapevines collected
from Vineyard 3 on 2 May 2013; bar = 1 cm (0.4 inch).
providing fewer areas of refuge for
these cryptic mites.
COMPARISON OF BLENDER
M ETH OD T O V ISU A L CO U N TS ON
•
February 2014 24(1)
DORMANT BUDS. The numbers of
grape rust mites overwintering in or
around single buds on dormant canes
were highly variable with respect to
bud position (Table 4). Relatively
high numbers of grape rust mites
were found in buds at any node along
the total length of the dormant cane.
The highest number of grape rust
mites found in any single bud using
the blender method was 483. The
blender method was most effective
in estimating grape rust mites in buds,
with 5-fold greater numbers of grape
rust mites found per bud compared
with visual counts under the stereoscope. It should be noted that no time
limit was applied when counting grape
rust mites visually for buds, so the direct
counts were not limited by observer
time. Grape rust mites observed visually
were often seen among the trichomes,
at the base of the bud beneath the first
few bud scales, or within the spongy
sclerenchyma tissues around the leaf
scar. The blender method was more
time-consuming to obtain grape rust
mite counts per sample than the RIB
method used earlier for shoots or leaves
because of extra plant debris released
during the blending step. The high
numbers of grape rust mites found in
buds at this site did not lead to significant stunting of shoots observed in the
following spring.
A CASE STUDY OF GRAPE RUST
MITE SEASONAL POPULATIONS. The
number of grape rust mites present
and symptoms on ‘Chardonnay’
shoots and leaves from Vineyard 2
was quite different in 2011 than in
2012 (Fig. 4). These data were collected from random samples in the
field so that the population estimates
would not be biased by collecting
shoots or leaves expressing symptoms
related to grape rust mite feeding. In
both years, the number of grape rust
mites detected on newly emerging
shoots was not different (P > 0.05).
However in 2011, the grape rust mite
population on leaves increased by
early summer and continued to increase until mid-September. Postharvest sampling in October yielded
relatively high numbers of grape rust
mites on leaves. In 2012, the population of grape rust mites did not
become established to any extent on
leaves and no stippling symptoms
were observed; the highest number
per leaf in mid-June 2012 was 1.2
grape rust mites. In 2011, the stippling symptoms were first observed
on leaves in this vineyard 2 weeks
before bloom and throughout the
rest of the growing season. Neither
43
RESEARCH REPORTS
Table 3. Effect of extraction and enumeration method on the mean number of grape rust mites, and effect of shoot type on the
mean number of fauna from individual young shoots of ‘Chardonnay’ grapevines from Vineyard 2 and ‘Syrah’ grapevines
from Vineyard 3 in Spring 2012.
Vineyard/date
‘Chardonnay’/ 30 Apr. 2012 15 d after
budbreak (n = 14)
‘Syrah’/2 May 2012 10 d after
budbreak (n = 10)
Variable
Grape rust mites-visual counts (no.)
Grape rust mites-RIB method (no.)x
Grape rust mites-RIB + blender method (no.)
Grape rust mites recovered by RIB method (%)
Predatory mites-RIB method (no.)w
Western flower thrips-RIB method (no.)w
Shoot length (cm)u
Grape rust mites-visual counts (no.)
Grape rust mites-RIB method (no.)
Grape rust mites-RIB + blender method (no.)
Grape rust mites recovered by RIB method (%)
Predatory mites-RIB method (no.)
Western flower thrips-RIB method (no.)
Shoot length (cm)
Shoot type
Normal
Stunted
P levelz
1.2 By
10.4 A
13.9 A
81.0
3.3 av
2.0
8.9 a
1.1 b, B
9.4 b, AB
29.3 b, A
39.9
0.2
1.6 b
4.7
0.082*
0.079*
0.069*
0.233
0.001*
0.699
<0.001
<0.001*
<0.001*
<0.001*
0.293
0.627
0.034
0.114
4.6 B
35.4 A
71.8 A
68.8
0.7 b
2.4
4.0 b
42.8 a, B
161.1 a, AB
482.1 a, A
34.8
0.3
4.9 a
4.0
z
Probability values followed by * were derived from Kruskal–Wallis analysis, all others from analysis of variance.
Means for grape rust mites determined by each method followed by a different capital letter within a column differ based on Kruskal–Wallis (K-W) multiple range test at 95%
confidence.
x
RIB = rinse in bag.
w
Predatory mites and western flower thrips were recorded for the RIB method only.
v
Means for shoot type followed by a different small case letter within a row differ based on Tukey’s honestly significant difference test or K-W multiple range test at 95%
confidence.
u
1 cm = 0.3937 inch.
y
stunted pubescent shoots (early season) nor leaf bronzing symptoms
(late season) were observed at Vineyard 2 in either year.
A CASE STUDY OBSERVING THE
IMPACT FROM SPRAYS ON GRAPE RUST
MITES. A midsummer sulfur application applied at Vineyard 1 reduced
grape rust mites on leaves in midSeptember by 80%, although vines
treated with potassium salts of fatty
acids did not differ from the nontreated vines (Table 5). The vineyard
manager also examined hundreds of
leaves throughout this block on 29
Aug. 2011 and recorded a decrease in
grape rust mite counts in the sulfurtreated plot but no decrease in the
plot treated with potassium salts of
fatty acids or the nontreated plot. Leaf
bronzing was visible by late Summer/
early Fall of 2011, and was less prevalent in the sulfur-treated plot. Rates of
single leaf photosynthesis were reduced
(P < 0.01) by 44% in bronzed leaves as
compared with nonsymptomatic leaves
measured on 22 Sept. 2011, although
location in the canopy (mid vs. upper)
was not significant. The assimilation
rate of nonsymptomatic and bronzed
leaves was (mean ± SE) 9.4 ± 1.0 and
5.3 ± 1.0 mmol CO2 fixed per square
meter per second, respectively.
Grape rust mites were observed
at Vineyard 1 by the vineyard manager
44
in early Spring 2012 during budbreak
and post-budbreak. As a result, the
vineyard manager increased sulfur use
to control grape rust mites as part of
his fungicide spray program throughout the 2012 growing season. This
resulted in decreased grape rust mite
populations and no leaf symptoms in
2012, as determined by the vineyard
manager.
Discussion
The primary purpose of this research was to develop a user-friendly
method to monitor grape rust mites
on leaves and shoots throughout the
year. The RIB method was quick and
effective for monitoring grape rust
mites on individual leaves (Tables 1,
2, and 5). Supplies needed for the
RIB method are readily available at
grocery or variety stores, except for
a moderate quality stereoscope required to examine extracts. High
numbers of grape rust mites were
recovered in the first wash from single
leaves (Fig. 1), and both ethanol and
isopropanol were effective in recovering grape rust mites from leaves. Reducing the concentration of alcohol
from 70% to 35% was equally as effective for extracting grape rust mites
from leaf surfaces (Table 1). The RIB
method is easier for viticulturists or
IPM consultants to accomplish than
the modified S&S method. Using a
single leaf with the RIB method is also
advantageous for three reasons: 1)
fewer laboratory supplies are needed,
2) little plant debris is extracted from
single leaves that allows for more
accurate enumeration under a stereoscope, and 3) a lower volume of
alcohol is used.
The RIB method was not as
efficient in extracting grape rust mites
from young shoots with numerous
trichomes (Table 3) as it was for fully
expanded leaves (Fig. 1). Difficulty
extracting eriophyoid mites from plant
surfaces with a high trichome density is
well known (Duso and Vettorazzo,
1999; Monfreda et al., 2010). The
lower efficiency of grape rust mite
extraction using the RIB method for
young ‘Syrah’ shoots compared with
young ‘Chardonnay’ shoots was most
likely because of the higher trichome
density on the former shoots (Table
3). However, the RIB method was less
time-consuming than visual counts or
blender extraction. For diagnosing
grape rust mite presence associated
with early season shoot stunting, all
three methods tested, including visual
counts under a stereoscope, gave similar results (Table 3). On the basis of 4
years of visual observations under a stereoscope across 15 vineyards, we have
had little difficulty diagnosing when
•
February 2014 24(1)
Table 4. Effect of extraction and enumeration method on the mean number of
grape rust mites associated with individual dormant buds of ‘Chardonnay’
grapevines from Vineyard 2 on 13 Jan. 2012.
Grape rust mites (no/bud)z
Visual counts
Blender counts
Bud
positiony
1
2
3
4
5
6
7
8
9
10
11
12
13
14
Total (all buds)
Range of values
6.8
5.0
30.2
35.0
13.3
18.5
51.0
14.0
11.0
2.0
0.3
18.8
11.1
2.5
16.0 bx
0–147
144.0
182.0
168.5
116.0
64.0
61.8
35.0
37.8
38.5
18.3
14.5
92.5
80.5
26.0
77.1 a
0–483
Buds analyzed
(no.)x
P level
4
4
4
4
4
4
4
4
4
4
4
4
4
4
56
0.236
0.191
0.309
0.375
0.191
0.166
0.885
0.375
0.245
0.081
0.091
0.166
0.248
0.663
<0.001
z
Different canes were used for each method because buds were destroyed.
Bud position is from the basal end of the cane.
Means followed by a different letter in a row differ based on Kruskal–Wallis multiple range test at 95%
confidence.
y
x
Fig. 4. Seasonal population of grape rust mites found on individual ‘Chardonnay’
grapevine shoots and leaves in 2011 and 2012 extracted using the rinse in bag
method. The first value in each year indicated within parentheses represents the
number of grape rust mites per shoot, all other values are per leaf (n = 20). Data are
means (±SE), and both years are shown at same scale. Arrows indicate the time of
wettable sulfur applications [4 lb/acre (4.5 kghaL1) actual sulfur] and an asterisk
(*) indicates that lime sulfur was included in a given spray at 0.2 gal/acre (1.9
LhaL1). Shoots or leaves were collected from Vineyard 2.
•
February 2014 24(1)
early spring shoot stunting was caused
by grape rust mites, as high numbers
of mites (always >200) were quickly
found upon examination under
a stereoscope.
Using the extraction methods
proved helpful in confirming grape
rust mite presence in symptomatic
vineyards. In the young ‘Syrah’ shoots
from Vineyard 3 where shoot-stunting
symptoms were evident, we found
160 grape rust mites per shoot using
the RIB method, which equated to
nearly 500 grape rust mites per
stunted shoot in total (RIB + blender
method). This is consistent with grape
rust mite numbers found with restricted spring growth research from
Australia and Europe (Bernard et al.,
2005; Duso and de Lillo, 1996), but
well above the proposed threshold of
nine grape rust mites per shoot
reported by Walton et al. (2010).
Further work will be required to establish distinct management thresholds for grape rust mites. However,
because both shoot expansion and
mite populations are in constant flux
early season, this goal may prove difficult to accomplish.
Scouting for visual symptoms
such as leaf stippling in grapevine
canopies can be a useful first step in
identifying emerging grape rust mite
outbreaks. The presence of leaf stippling was the first symptom expressed
in grape rust mite-infested experimental vines (nursery cuttings), newly
planted vineyards, and established
vineyards across the region, even before spring shoot stunting had occurred typically the following year. A
clear association of grape rust mite
numbers per leaf and stippling symptoms was shown in early summer
(Fig. 2), and also at the end of summer
(mid-September) when leaves collected at random were compared with
leaves selected with stippling symptoms (Table 2). Leaf stippling was also
found in all the vineyards sampled
during summer months over the past
4 years where significant grape rust
mite populations have been identified
(R.P. Schreiner and P.A. Skinkis, unpublished data). Leaf stippling symptoms have been noted in other reports
from Europe (Estación Fitopatolóxica
do Areeiro, 2013; Vinograd, 2013).
Late-season leaf bronzing symptoms
that result from heavy grape rust mite
infestations are well known (Baillod
and Guignard, 1986; Duso et al.,
45
RESEARCH REPORTS
Table 5. Impact of wettable sulfur or potassium salts of fatty acids sprays from
a nonreplicated case study on the mean number of fauna extracted from
individual leaves of ‘Pinot noir’ grapevines from Vineyard 1 on 19 Sept. 2011.
Treatmentz
Wettable sulfur
Potassium salts of fatty acids
Nontreated
P level
Grape rust
mites (no.)
818 by
2958 a
4447 a
0.009
Predatory
mites (no.)
2b
7a
5a
0.002
Western flower
thrips (no.)
4
3
5
0.226
z
Leaves were collected at random 1 mo. after spray application and extracted using the rinse in bag method (n =
15). Wettable sulfur = 5 lb/acre (5.6 kgha–1) actual sulfur, potassium salts of fatty acids = 0.75 gal/acre (7.0
Lha–1) a.i., nontreated = no miticide application.
y
Means followed by a different letter within a column differ based on Tukey’s honestly significant difference test at
95% confidence.
2010), but this symptom may not
occur in all vineyards. The simultaneous occurrence of both stippling
and bronzing symptoms on leaves, as
seen at Vineyard 1 in 2011, clearly
indicates a high grape rust mite population. At Vineyard 1, the bronzing
was more apparent on the older leaves
although stippling was more noticeable
on younger, upper canopy leaves, suggesting that bronzing requires greater
exposure time to grape rust mites in
order to develop. It should be noted
that western flower thrips can cause
a similar type of shoot and leaf damage
on grapevines, but the symptoms can
be distinguished by the larger size of
translucent zones on the leaf and the
formation of necrotic lesions on the leaf
surface mid- to late season. These larger
clear zones on leaves caused by western
flower thrips feeding are typically located near intersections of major leaf
veins and often near the petiole. In
comparison, grape rust mites produce
smaller stippling clear zones (pinhole
size) and they are typically scattered
across much of the leaf surface (Fig. 2).
The high number of grape rust
mites on leaves (>3000 per leaf) observed at the severely infested Vineyard
1 in 2011 was similar to the highest
levels of grape rust mites reported in
Europe (Duffner et al., 2001; Duso
and de Lillo, 1996; Pérez-Moreno and
Moraza-Zorrilla, 1998). The populations at Vineyard 2 in 2011, which we
consider a moderate infestation (400
grape rust mites per leaf), were higher
than those reported in earlier work
conducted in Oregon (Walton et al.,
2007, 2010) and Europe (Hluchý and
Pospišil, 1992) where crop yield was
reported to be reduced. No evidence
of crop loss or stunted shoots was
found in Vineyard 1 or Vineyard 2 in
2011 or in 2012 (data not shown),
46
suggesting that damage thresholds for
this pest in a given vineyard may vary
considerably. A decline in grape rust
mite populations on leaves at the end
of summer was not apparent in either
Vineyard 1 or Vineyard 2 in 2011 as
reported in other studies (Duso and
de Lillo, 1996; Pérez-Moreno and
Moraza-Zorrilla, 1998). Similar to our
findings, Walton et al. (2007) reported
that leaf populations of grape rust
mites did not decrease at the end of
the summer. These results suggest that
a large migration of grape rust mites to
overwintering sites near the base of
shoots or trunks of vines may not
occur as early in summer as suggested
earlier (Pérez-Moreno and MorazaZorrilla, 1998) or may not occur
consistently in all vineyards.
Analysis of single leaf gas exchange at Vineyard 1 in late Summer
2011 showed that photosynthesis was
reduced by 44% in bronzed leaves as
compared with asymptomatic leaves.
The rate of photosynthesis of bronzed
grapevine leaves caused by grape rust
mites did not differ from nonsymptomatic leaves in Germany (Rees and
Scruft, 1994). However, leaf photosynthesis and transpiration were reduced in apple (Malus ·domestica)
leaves infested by the apple rust mite
[Aculus schlechtendali (Spieser et al.,
1998)]. Our data suggest that high
populations of grape rust mites can
reduce photosynthesis and explain perhaps why reduced sugar accumulation
in berries has occurred in severely
infested vineyards (Hluchý and Pospišil,
1992). Low sugar concentration in
berries was reported by the vineyard
manager of Vineyard 1 in 2011.
Appropriately timed canopy sulfur applications appear to be an effective tool in managing grape rust mite
populations during the growing
season. The divergent grape rust mite
populations quantified over two seasons at Vineyard 2 are likely related to
increased sulfur use in 2012 (Fig. 4).
The two canopy sulfur applications
aimed toward controlling grape rust
mites during wooly bud stage before
budbreak in 2011 (containing lime
sulfur and wettable sulfur) did not
appear to control grape rust mites
that year. This could be due to the
2-month time lapse between subsequent sulfur applications, allowing
a small population to multiply rapidly
by early summer. In 2012, the grape
rust mite population never accrued on
leaves during summer, which appears
to be due to the more timely use of
sulfur by the vineyard manager for
dual use as a miticide and fungicide to
control grape powdery mildew (Erisyphe necator). Sulfur applications
were more numerous and spray intervals were shorter in 2012 than in
2011 (Fig. 4). A single midsummer
sulfur application at Vineyard 1 also
reduced grape rust mites on leaves by
80%, although potassium salts of
fatty acids did not reduce populations
(Table 5). Seasonal populations of
grape rust mites studied over 4 years
in a Spanish vineyard support our
findings to some degree (PérezMoreno and Moraza-Zorrilla, 1998).
They reported the lowest population of
grape rust mites on leaves when three
closely timed sulfur applications were
applied to the canopy in early summer,
although higher populations were
found in the years where only one or
two sulfur applications were made.
These findings combined with
experiences from multiple grower’s
in Oregon using wettable sulfur indicate that sulfur is a promising tool
for reducing grape rust mite populations. The utility of sulfur for controlling grape rust mites is also supported
by our observations of where grape
rust mite outbreaks have typically occurred in the region. Grape rust mite
problems and symptoms of shoot
stunting, leaf stippling, or leaf bronzing have most often been found in
newly planted vineyards that do not
have a fully implemented spray program or in older (producing) vineyards where sulfur use has been
largely replaced by synthetic fungicides for grape powdery mildew control in the Willamette Valley.
Estimating grape rust mite presence in winter may also be useful for
•
February 2014 24(1)
early season management, before
symptoms are visible. The blender
method used in this study was more
effective than visual counts under
a stereoscope for estimating grape
rust mites overwintering in or around
dormant buds. The number of grape
rust mites found in buds was much
greater than earlier reports (Bernard
et al., 2005; Walton et al., 2007).
However, despite the high numbers
of grape rust mites observed in buds
from Vineyard 2 during Winter 2012,
only low numbers of grape rust mites
were found on shoots the following
spring. Therefore, a decline of grape
rust mites in late winter/early spring
had occurred because of unknown factors. It should be noted that no early
season (wooly bud or post-budbreak)
lime sulfur was applied in 2012 to
explain this population decline. It is
likely that high numbers of grape rust
mites per bud in the winter are necessary to reliably predict if shoot stunting will occur the following spring.
On the basis of Vineyard 2 data, an
average of 77 grape rust mites per bud
in winter did not cause shoot stunting
the following spring. Understanding
the biotic and abiotic factors that
impact the survival of grape rust mites
from midwinter to early spring within
grapevine buds is an important area
for future research.
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